Evo-Devo

What is Evo-Devo?

Molecular developmental biology and evolutionary molecular genetics have proven, these last 20 years, to be highly successful but, strangely enough, remained largely separated despite the obvious conceptual links between the two disciplines. Indeed, on one hand, molecular developmental biologists have focused on the use of a handful of model organisms (such as the nematode Caenorhabditis elegans, the fruitfly Drosophila melanogaster, the frog Xenopus tropicalis/laevis, and the laboratory mouse Mus musculus) for deciphering the fascinating processes by which cells differentiate, as well as tissues, organs, and organisms grow and develop. On the other hand, evolutionary molecular geneticists have investigated the modes and tempos of DNA and protein evolution in a multitude of organisms (from viruses to vertebrates), and developed the laboratory techniques and analytical methods allowing today to infer phylogenies, reconstruct population histories, uncover hidden biodiversity, and detect selection and stochastic patterns in laboratory and natural populations.

Given that a large proportion of evolutionary mechanisms, namely, those pertaining to natural selection, act on the phenotypes that originate from development (i.e., genetic information and epigenetic parameters are translated into phenotypes during development), it was fully realized only in the 1990’s, that our understanding of both evolution and development would greatly benefit from the partial merging of the two above-mentioned disciplines into what is called today Evolutionary Developmental Biology (EVO-DEVO). This emerging approach has been recently recognised as a new and innovative discipline by the Academy of Sciences of the USA. The motivation of synthesizing findings from molecular developmental biology and evolutionary biology already yielded some spectacular results as, e.g., illustrated by the partial understanding of Hox gene involvement in the origin and evolution of characters, such as appendages and segmentation, across lineages. The existence of identical signals for the, supposedly independent, development of structures of similar functions (e.g., the eye) in very different lineages, has shaken concepts as central/major as homology. The significance of the new field of Evo-Devo is demonstrated by the recent establishment of specialized journals (e.g., Evolution & Development; Molecular and Developmental Evolution) and university chairs of evolutionary developmental biology are being established at an accelerated pace, especially in the US and the UK.

The most important defining feature of Evo-Devo is that it explicitly addresses the generative mechanisms underlying the evolution of organismal forms on both short-term and long-term timescales. Uncovering these mechanisms will require the use of many additional model organisms. Evo-Devo studies are, by essence, highly multidisciplinary and integrative as they require investigation, across lineages, of morphological/ physiological, as well as of the underlying genomic, characters. Many recent and powerful concepts such as the self-organizational capabilities of cells and tissues, the dynamics of epigenetic interactions among developmental modules, the role of geometry and form in developmental and evolutionary processes (extending also into the field of theoretical biology), are pertinent for addressing the causal and reciprocal interrelations between development and evolution at multiple scales and multiple levels of analysis. Evo-Devo also requires diversity in the taxa analysed, in the levels of analysis (from the gene – identification, expression, control - to the developmental mechanisms to the phenotype), and in the techniques used (the expression analysis and RNAi/morpholinos technologies from developmental genetics, and the genomic/analytical technologies from evolutionary genetics).

We recently developed multiple non-classical model systems in vertebrates for Evo-Devo studies. Currently, our major interests revolve around two topics: uncovering the genetic basis of (i) evolutionary novelties and of (ii) phenotypic convergences.

Non-classical model systems

The criteria that are relevant to the choice of a set of model species are multiple and can even be contradictory. We think that the only possibility is the use of a pragmatic (and partly subjective) optimisation approach, incorporating multiple criteria. We have applied such an approach for a set of species that could serve as the workhorses for evo-devo research within amniotes. We use these species in our laboratory for studying the Evo-Devo of phenotypic novelties and convergences, using classical developmental and molecular genetics methods (in-situ hybridization, DNA arrays, library building and sequencing, etc.).

Additional information is available HERE.

Lineage-specific novelties

Increase of complexity is certainly not a universal law of evolution. Indeed, multiple lineages, such as myzostomes and flatworms, probably exhibit derived (rather than ancestral), simplified body plans. Still, it is undisputable that some lineages in the phylogenetic tree of life are characterized by the accelerated acquisition of new and complex physiological and morphological characters. Some obvious examples include the origin of chromosomes, the origin of eukaryotes, the origin of sex, the origin of multicellularity, the origin of social groups, etc.  At a finer phylogenetic scale, examples of accelerated anagenesis can be found in vertebrates as well, especially at the origin of tetrapods, of mammals, and of birds. It is the accelerated rate of morphological/physiological evolution of the latter two lineages that explains the paraphyly of “reptiles” (exposed in basically every text book on evolution). Although the absolute amount of DNA in a haploid cell (the so called “c-value”) is very poorly correlated with organismal complexity, it is likely that at least some macroevolutionary events are due to the emergence of new genes or gene families. It is generally believed that some of the acquisitions of new genes (through duplications, retropositions, etc.) are correlated to at least some of the well-accepted major transitions of complexity in evolution. This project aims at identifying some of the gene acquisitions that are associated with evolutionary morphological and physiological transitions in selected internal branches of the vertebrate phylogenetic tree.

We approach this issue from two different avenues:

1. (i)Experimental identification of the molecular generative mechanisms of lineage-specific phenotypes (cf. above, check for details HERE)
   

2. (ii)Evolutionary comparative genomics, i.e., in-silico comparative analysis of full genomes in a phylogenetic framework (check for details HERE). 
   

Lineage-specific novelties: (3) in between top & down

Comparison of the transcriptome across species should be one of the best approaches for understanding the genetic basis of phenotype differences among evolutionary lineages. The past decade has seen the development of new techniques to study the transcriptome. The most popular are: (1) serial analysis of gene expression (SAGE), (2) sequencing of expressed sequence tags (ESTs), (3) substractive hybridization, (4) differential display, and (5) microarrays. Subtractive hybridization methods are useful for isolating up- or down-regulated transcripts using reassociation kinetics, but are technically demanding. Differential display is a straightforward modification of RAPDs methods using RNA as template, but the downstream procedures to isolate cDNAs of interest normally lead to large numbers of false positives. Subtractive hybridization and differential display can both be used to isolate transcripts showing large differences in abundance between two samples, but are not useful for quantifying precisely the relative amounts of differentially expressed genes on a genomic scale. The microarray technology is the most useful high-throughput tool with which to conduct transcriptome analyses but are technically demanding when performed across distantly-related species and does not provide sequence information. SAGE and ESTs have the advantage to provide the sequence information (in addition to the expression information) and have had important roles in gene and exon discovery efforts, but are not suitable for routine comparative studies mainly because of the large expense inherent to sequencing thousands of clones or PCR products using classical molecular cloning in bacterial hosts and Sanger capillary sequencing technologies.

We are using the new sequencing technology (that associates pico-litter emulsion clonal amplification and pyrosequencing) from Roche / 454-life-sciences to the ultra-fast sequencing of full transcriptomes in multiple species, multiple organs and tissues, and multiple developmental stages. This approach will combine the advantages of high-throughput (similar to miroarrays) and of sequence information.

Stay tuned for additional information soon.

Selected publications

1. ✓Bossuyt F. & M. C. Milinkovitch
   Convergent Adaptive Radiations in Madagascan and Asian Ranid Frogs Reveal Co-variation between Larval and Adult Traits.
   PNAS 97: 6585-6590 (2000)
   

2. Open Access
   

3. ✓Cassens I., Vicario S., Waddell V. G., Balchowsky H., Van Belle D., Wang Ding, Chen Fan, Lal Mohan R.S., Simões-Lopes P. C., Bastida R., Meyer A., Stanhope M. J. & M. C. Milinkovitch.
   Independent Adaptation to Riverine Habitats Allowed Survival of Ancient Cetacean Lineages.
   

   

   PNAS, 97: 11343-11347 (2000)
   

4. Open Access
   

5. ✓Milinkovitch M.C. & A. C. Tzika
   Escaping the Mouse Trap; the Selection of New Evo-Devo Model Species
   Journal of Experimental Zoology (Mol. Dev. Evol.) 308B: 337–346 (2007)
   

6. e-mail
   

7. News Coverage
   

8. ✓Tzika A. C. & M. C. Milinkovitch.
   A Pragmatic Approach for Selecting Evo-Devo Model Species in Amniotes
   Chapter 7 Pages 119-140 in ‘Evolving Pathways; Key Themes in Evolutionary Developmental Biology’ (A. Minelli & G. Fusco, eds.), Cambridge University Press 2008
   

9. e-mail
   

10. ✓Tzika A. C., Helaers R., Van de Peer Y. & M. C. Milinkovitch
    MANTiS: a phylogenetic framework for multi-species genome comparisons
    Bioinformatics, 24 (2):151-157 (2008)
    

11. Open Access: article
    

12. OpenAccess: supplementary material
    

13. Download the MANTiS software
    

14. ✓Milinkovitch M.C., Helaers R., & A.C. Tzika
    Historical Constraints on Vertebrate Genome Evolution
    Genome Biololgy & Evolution 2010: 13-18 (2010)
    

15. Open Access
    

16. ✓Milinkovitch M.C., Helaers R., Depiereux E., Tzika A.C., & T. Gabaldon
    2X genomes - depth does matter
    Genome Biology, 11 (2): R16 (2010)
    

17. Open Access
    

18. ✓Di-Poï N., Montoya-Burgos J.I., Miller H., Pourquié O., Milinkovitch M.C. & D. Duboule
    Changes in Hox genes’ structure and function during the evolution of the squamate body plan
    Nature, 464: 99-103 (2010)
    

19. e-mail: Article
    

20. e-mail: Supplementary File
    

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